Lipoxins and aspirin-triggered 15-epi-lipoxin biosynthesis: An update and role in anti-inflammation and pro-resolution

Prostaglandins and Other Lipid Mediators

Volumn 68-69, Issue , 2002, Pages 433-455

  Serhan, Charles N ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anti inflammation; Leukocytes; Platelets; Resolution mediators; Signal transduction

Indexed keywords

15 EPILIPOXIN DERIVATIVE; ACETYLSALICYLIC ACID; ANTIINFLAMMATORY AGENT; LIPOXIN DERIVATIVE; UNCLASSIFIED DRUG; ARACHIDONATE 5 LIPOXYGENASE; HYDROXYICOSATETRAENOIC ACID; LEUKOTRIENE; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTAGLANDIN;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTHMA; CELL INTERACTION; DRUG MECHANISM; LEUKOCYTE; LEUKOCYTE MIGRATION INHIBITION; LIPOGENESIS; NEUTROPHIL; NONHUMAN; ORGAN INJURY; SIGNAL TRANSDUCTION; ANIMAL; CELL ADHESION; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ARACHIDONATE 5-LIPOXYGENASE; ASPIRIN; ASTHMA; CELL ADHESION; HUMANS; HYDROXYEICOSATETRAENOIC ACIDS; INFLAMMATION; LEUKOCYTES; LEUKOTRIENES; MOLECULAR STRUCTURE; PROSTAGLANDINS;

EID: 0036669399     PISSN: 00906980     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0090-6980(02)00047-3     Document Type: Article

References (115)

1. Gallin JI, Snyderman R, Fearon DT, Haynes BF, Nathan C, editors. Inflammation: Basic Principles and Clinical Correlates. Philadelphia: Lippincott Williams & Wilkins, 1999.
2. Samuelsson B., Dahlén S.E., Lindgren J.Å., Rouzer C.A., Serhan C.N. Leukotrienes and lipoxins: structures biosynthesis and biological effects. Science. 237:1987;1171.
3. Cronstein B.N., Montesinos M.C., Weissmann G. Sites of action for future therapy: an adenosine-dependent mechanism by which aspirin retains its antiinflammatory activity in cyclooxygenase-2 and NFkB knockout mice. Osteoarthritis Cartilage. 7:1999;361.
4. Cronstein B.N., Montesinos M.C., Weissmann G. Salicylates and sulfasalazine, but not glucocorticoids, inhibit leukocyte accumulation by an adenosine-dependent mechanism that is independent of inhibition of prostaglandin synthesis and p105 of NFκB. Proc. Natl. Acad. Sci. USA. 96:1999;6377.
5. Krump E., Picard S., Mancini J., Borgeat P. Suppression of leukotriene B4 biosynthesis by endogenous adenosine in ligand-activated human neutrophils. J. Exp. Med. 186:1997;1401.
6. Qiu F.-H., Wada K., Stahl G.L., Serhan C.N. IMP and AMP deaminase in reperfusion injury down-regulates neutrophil recruitment. Proc. Natl. Acad. Sci. USA. 97:2000;4267.
7. Serhan C.N. Lipoxin biosynthesis and its impact in inflammatory and vascular events. Biochim. Biophys. Acta. 1212:1994;1.
8. Serhan C.N., Haeggström J.Z., Leslie C.C. Lipid mediator networks in cell signaling: update and impact of cytokines. FASEB J. 10:1996;1147.
9. de Waal Malefyt R. Inflammation: Basic Principles and Clinical Correlates. In: Gallin JI, Snyderman R, Fearon DT, Haynes BF, Nathan C, editors. Philadelphia: Lippincott Williams & Wilkins, 1999. p. 837.
10. Diamond P., McGinty A., Sugrue D., Brady H.R., Godson C. Regulation of leukocyte trafficking by lipoxins. Clin. Chem. Lab. Med. 37:1999;293.
11. Marcus A.J. Aspirin as prophylaxis against colorectal cancer. N. Engl. J. Med. 333:1995;656.
12. Vane JR. Les Prix Nobel: Nobel Prizes, Presentations, Biographies and Lectures. Stockholm: Almqvist & Wiksell, 1982. p. 181.
13. 4 ELISA. J. Pharmacol. Exp. Ther. 287:1998;779.
14. Clària J., Serhan C.N. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc. Natl. Acad. Sci. USA. 92:1995;9475.
15. Clària J., Lee M.H., Serhan C.N. Aspirin-triggered lipoxins (15-epi-LX) are generated by the human lung adenocarcinoma cell line (A549)-neutrophil interactions and are potent inhibitors of cell proliferation. Mol. Med. 2:1996;583.
16. 4. FASEB J. 15:2001;A949.
17. Showell HJ, Cooper K. Inflammation: Basic Principles and Clinical Correlates. In: Gallin JI, Snyderman R, editors. Philadelphia: Lippincott Williams & Wilkins, 1999. p. 1177.
18. Malaviya R., Abraham S.N. Role of mast cell leukotrienes in neutrophil recruitment and bacterial clearance in infectious peritonitis. J. Leukoc. Biol. 67:2000;841.
19. Swan S.K., Rudy D.W., Lasseter K.C., Ryan C.F., Buechel K.L., Lambrecht L.J.et al. Effect of cyclooxygenase-2 inhibition on renal function in elderly persons receiving a low-salt diet: a randomized controlled trial. Ann. Intern. Med. 133:2000;1.
20. Cannon G.W., Caldwell J.R., Holt P., McLean B., Seidenberg B., Bolognese J.et al. Rofecoxib, a specific inhibitor of cyclooxygenase 2, with clinical efficacy comparable with that of diclofenac sodium: results of a one-year, randomized, clinical trial in patients with osteoarthritis of the knee and hip. Rofecoxib Phase III Protocol 035 Study Group. Arthritis Rheum. 43:2000;978.
21. 4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry. 34:1995;14609.
22. Serhan C.N. Lipoxins and novel aspirin-triggered 15-epi-lipoxins (ATL): a jungle of cell-cell interactions or a therapeutic opportunity? Prostaglandins. 53:1997;107.
23. Levy B.D., Clish C.B., Schmidt B., Gronert K., Serhan C.N. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2:2001;612.
24. 4 up-regulate transcriptional corepressor NAB1 in human neutrophils. FASEB J October 29, 2001, 10. 1096/fj. 01-0576fje (available at www.fasebj.org).
25. Varani J., Ward P.A. Mechanism of neutrophil-dependent and neutrophil-independent endothelial cell injury. Biol. Signals. 3:1994;1.
26. 4 by platelet 12-lipoxygenase in vitro. J. Clin. Invest. 85:1990;772.
27. Edenius C., Stenke L., Lindgren J.A. On the mechanism of transcellular lipoxin formation in human platelets and granulocytes. Eur. J. Biochem. 199:1991;401.
28. Lehr H.-A., Frei B., Arfors K.-E. Vitamin C prevents cigarette smoke-induced leukocyte aggregation and adhesion to endothelium in vivo. Proc. Natl. Acad. Sci. USA. 91:1994;7688.
29. Brady H.R., Serhan C.N. Adhesion promotes transcellular leukotriene biosynthesis during neutrophil-glomerular endothelial cell interactions: inhibition by antibodies against CD18 and L-selectin. Biochem. Biophys. Res. Commun. 186:1992;1307.
30. Herschman H.R. Recent progress in the cellular and molecular biology of prostaglandin synthesis. Trends Cardiovasc. Med. 8:1998;145.
31. Samuelsson, B. Les Prix Nobel: Nobel Prizes, Presentations, Biographies and Lectures. Stockholm: Almqvist & Wiksell, 1982. p. 153.
32. Serhan C.N., Prescott S.M. The scent of a phagocyte: advances on leukotriene B4 receptors. J. Exp. Med. 192:2000;F5.
33. 4 and epoxytetraenes: stabilization of eicosanoids by liposomes. Biochem. Biophys. Res. Commun. 159:1989;477.
34. Nassar G.M., Morrow J.D., Roberts L.J II, Lakkis F.G., Badr K.F. Induction of 15-lipoxygenase by interleukin-13 in human blood monocytes. J. Biol. Chem. 269:1994;27631.
35. Levy B.D., Romano M., Chapman H.A., Reilly J.J., Drazen J., Serhan C.N. Human alveolar macrophages have 15-lipoxygenase and generate 15(S)-hydroxy-5,8,11-cis-13-trans-eicosatetraenoic acid and lipoxins. J. Clin. Invest. 92:1993;1572.
36. Levy G.N. Prostaglandin H synthases, nonsteroidal anti-inflammatory drugs, and colon cancer. FASEB J. 11:1997;234.
37. Savage M.P., Goldberg S., Bove A.A., Deutsch E., Vetrovec G., Macdonald R.G.et al. Effect of thromboxane A2 blockade on clinical outcome and restenosis after successful coronary angioplasty. Circulation. 92:1995;3194.
38. Sneader W. The discovery of aspirin: a reappraisal. BMJ. 321:2000;1591.
39. 4 and N-formyl-L-methionyl-L-leucyl-L-phenylalanine. Clin. Sci. 77:1989;195.
40. 4 inhibit leukotriene-stimulated interactions of human neutrophils and endothelial cells. J. Immunol. 156:1996;2264.
41. 4 inhibit tumor necrosis factor 1α-initiated neutrophil responses and trafficking: regulators of a cytokine-chemokine axis. J. Exp. Med. 189:1999;1923.
42. 4 modulates transmigration of human neutrophils across intestinal epithelial monolayers. J. Clin. Invest. 92:1993;75.
43. 4 stable analogs are potent inhibitors of acute inflammation: evidence for anti-inflammatory receptors. J. Exp. Med. 185:1997;1693.
44. 4 stable analogues. J. Clin. Invest. 101:1998;819.
45. Clish C.B., O'Brien J.A., Gronert K., Stahl G.L., Petasis N.A., Serhan C.N. Local and systemic delivery of a stable aspirin-triggered lipoxin prevents neutrophil recruitment in vivo. Proc. Natl. Acad. Sci. USA. 96:1999;8247.
46. 4 accelerate resolution of allergic edema in Angiostrongylus costaricensis-infected rats: relationship with concurrent eosinophilia. J. Immunol. 164:2000;1029.
47. Chiang N., Gronert K., Clish C.B., O'Brien J.A., Freeman M.W., Serhan C.N. Leukotriene B4 receptor transgenic mice reveal novel protective roles for lipoxins and aspirin-triggered lipoxins in reperfusion. J. Clin. Invest. 104:1999;309.
48. 4 analogs. J. Clin. Invest. 101:1998;1860.
49. 4 and regulation of vascular and inflammatory responses. Am J Pathol 2001;158:3.
50. 4 inhibits cholinergic neurotransmission through nitric oxide generation in the rabbit trachea. Eur. J. Pharmacol. 287:1995;233.
51. Serhan C.N., Hamberg M., Samuelsson B. Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc. Natl. Acad. Sci. USA. 81:1984;5335.
52. Ford-Hutchinson A.W. Arachidonate 15-lipoxygenase characteristics and potential biological significance. Eicosanoids. 4:1991;65.
53. Sigal E., Conrad D.J. Human 15-lipoxygenase: a potential effector molecule for interleukin-4. Adv. Prostaglandin Thromboxane Leukot. Res. 22:1994;309.
54. Katoh T., Lakkis F.G., Makita N., Badr K.F. Co-regulated expression of glomerular 12/15-lipoxygenase and interleukin-4 mRNA in rat nephrotoxic nephritis. Kidney Int. 46:1994;341.
55. 2-like cells in allergy and asthma: pharmacological perspectives. Trends Pharmacol. Sci. 15:1994;324.
56. Pouliot M., McDonald P.P., Borgeat P., McColl S.R. Granulocyte/macrophage colony-stimulating factor stimulates the expression of the 5-lipoxygenase-activating protein (FLAP) in human neutrophils. J. Exp. Med. 179:1994;1225.
57. Ring W.L., Riddick C.A., Baker J.R., Munafo D.A., Bigby T.D. Lymphocytes stimulate expression of 5-lipoxygenase and its activating protein in monocytes in vitro via granulocyte-macrophage colony stimulating factor and interleukin-3. J. Clin. Invest. 97:1996;1293.
58. L'Heureux G.P., Bourgoin S., Jean N., McColl S.R., Naccache P.H. Diverging signal transduction pathways activated by interleukin-8 and related chemokines in human neutrophils: interleukin-8, but not NAP-2 or GROAa, stimulates phospholipase D activity. Blood. 85:1995;522.
59. 4: comparison of icosanoids having bronchoconstrictor and vasodilator actions but lacking platelet aggregatory activity. Proc. Natl. Acad. Sci. USA. 85:1988;8340.
60. Dahlén SE, Serhan CN. Lipoxygenases and Their Products. In: Wong A, Crooke ST, editors. San Diego: Academic Press, 1991. p. 235.
61. 4: structure-function relationships. Biochem. Biophys. Res. Commun. 180:1991;1416.
62. 4 in rat glomerular mesangial cells: evidence for competition at a common receptor. Proc. Natl. Acad. Sci. USA. 86:1989;3438.
63. Fiore S., Serhan C.N. Formation of lipoxins and leukotrienes during receptor-mediated interactions of human platelets and recombinant human granulocyte/macrophage colony-stimulating factor-primed neutrophils. J. Exp. Med. 172:1990;1451.
64. Chavis C., Chanez P., Vachier I., Bousquet J., Michel F.B., Godard P. 5,15-diHETE and lipoxins generated by neutrophils from endogenous arachidonic acid as asthma biomarkers. Biochem. Biophys. Res. Commun. 207:1995;273.
65. Chavis C., Vachier I., Chanez P., Bousquet J., Godard P. 15(S)-Dihydroxyeicosatetraenoic acid and lipoxin generation in human polymorphonuclear cells: dual specificity of 5-lipoxygenase towards endogenous and exogenous precursors. J. Exp. Med. 183:1996;1633.
66. Thomas E., Leroux J.L., Blotman F., Chavis C. Conversion of endogenous arachidonic acid to 5,15-diHETE and lipoxins by polymorphonuclear cells from patients with rheumatoid arthritis. Inflamm. Res. 44:1995;121.
67. Shen J., Herderick E., Cornhill J.F., Zsigmond E., Kim H.-S., Kühn H.et al. Macrophage-mediated 15-lipoxygenase expression protects against atherosclerosis development. J. Clin. Invest. 98:1996;2201.
68. Brezinski M.E., Serhan C.N. Selective incorporation of (15S)-hydroxyeicosatetraenoic acid in phosphatidylinositol of human neutrophils: agonist-induced deacylation and transformation of stored hydroxyeicosanoids. Proc. Natl. Acad. Sci. USA. 87:1990;6248.
69. Edenius C., Haeggström J., Lindgren J.A. Transcellular conversion of endogenous arachidonic acid to lipoxins in mixed human platelet-granulocyte suspensions [published erratum appears in Biochem Biophys Res Commun 28;159(1):370]. Biochem. Biophys. Res. Commun. 157:1988;801.
70. 4 transfer. Trends Pharmacol. Sci. 14:1993;351.
71. Corey E.J., Mehrotra M.M. A stereoselective and practical synthesis of 5,6(S,S)-epoxy-15(S)-hydroxy-7(E),9(E),11(Z),13(E)-eicosatetraenoic acid (4), possible precursor of the lipoxins. Tetrahedron Lett. 27:1986;5173.
72. Sheppard K.A., Greenberg S.M., Funk C.D., Romano M., Serhan C.N. Lipoxin generation by human megakaryocyte-induced 12-lipoxygenase. Biochim. Biophys. Acta. 1133:1992;223.
73. Romano M., Serhan C.N. Lipoxin generation by permeabilized human platelets. Biochemistry. 31:1992;8269.
74. Romano M., Chen X.S., Takahashi Y., Yamamoto S., Funk C.D., Serhan C.N. Lipoxin synthase activity of human platelet 12-lipoxygenase. Biochem. J. 296:1993;127.
75. Lehr H.A., Olofsson A.M., Carew T.E., Vajkoczy P., von Andrian U.H., Hübner C.et al. P-selectin mediates the interaction of circulating leukocytes with platelets and microvascular endothelium in response to oxidized lipoprotein in vivo. Lab. Invest. 71:1994;380.
76. Mayadas T.N., Mendrick D.L., Brady H.R., Tang T., Papayianni A., Assmann K.J.M.et al. Acute passive anti-glomerular basement membrane nephritis in P-selectin-deficient mice. Kidney Int. 49:1996;1342.
77. 4 during adhesion of platelets and neutrophils in experimental immune complex glomerulonephritis. Kidney Int. 47:1995;1295.
78. Garrick R., Wong P.Y. Enzymatic formation and regulatory function of lipoxins and leukotriene B4 in rat kidney mesangial cells. Adv. Exp. Med. Biol. 314:1991;361.
79. Edenius C., Kumlin M., Björk T., Anggard A., Lindgren J.A. Lipoxin formation in human nasal polyps and bronchial tissue. FEBS Lett. 272:1990;25.
80. Tornhamre S., Gigou A., Edenius C., Lellouche J.P., Lindgren J.A. Conversion of 5,6-dihydroxyeicosatetraenoic acids. A novel pathway for lipoxin formation by human platelets. FEBS Lett. 304:1992;78.
81. Rowley A.F., Hill D.J., Ray C.E., Munro R. Haemostasis in fish - an evolutionary perspective. Thromb. Haemost. 77:1997;227.
82. Gronert K., Virk S.M., Herman C.A. Thrombocytes are the predominant source of endogenous sulfidopeptide leukotrienes in the bullfrog (Rana catesbeiana). Biochim. Biophys. Acta. 1255:1995;311.
83. 4 receptor. J. Biol. Chem. 272:1997;6972.
84. Stenke L., Reizenstein P., Lindgren J.A. Leukotrienes and lipoxins - new potential performers in the regulation of human myelopoiesis. Leukemia Res. 18:1994;727.
85. 4 in the bronchoalveolar lavage fluids obtained from patients with selected pulmonary diseases. Am. Rev. Respir. Dis. 141:1990;1453.
86. 4-ELISA. Lipids. 28:1993;1047.
87. 4 Impact of aspirin therapy. Circulation. 86:1992;56.
88. 4 and decreased lipoxin formation in chronic myeloid leukemia. Adv. Prostaglandin Thromboxane Leukot. Res. 21B:1990;883.
89. Herschman H.R. Prostaglandin synthase 2. Biochim. Biophys. Acta. 1299:1996;125.
90. Xiao G., Tsai A.L., Palmer G., Boyar W.C., Marshall P.J., Kulmacz R.J. Analysis of hydroperoxide-induced tyrosyl radicals and lipoxygenase activity in aspirin-treated human prostaglandin H synthase-2. Biochemistry. 36:1997;1836.
91. Hennekens C., Jonas M., Buring J. The benefits of aspirin in acute myocardial infarction. Still a well-kept secret in the United States. Arch. Intern. Med. 154:1994;37.
92. Giovannucci E., Egan K.M., Hunter D.J., Stampfer M.J., Colditz G.A., Willett W.C.et al. Aspirin and the risk of colorectal cancer in women. N. Engl. J. Med. 333:1995;609.
93. Sanak M., Levy B.D., Clish C.B., Chiang N., Gronert K., Mastalerz L.et al. Aspirin-tolerant asthmatics generate more lipoxins than aspirin-intolerant asthmatics. Eur. Respir. J. 16:2000;44.
94. Clària J., Titos E., Jiménez W., Ros J., Ginès P., Arroyo V.et al. Altered biosynthesis of leukotrienes and lipoxins and host defense disorders in patients with cirrhosis and ascites. Gastroenterology. 115:1998;147.
95. Stenke L., Edenius C., Samuelsson J., Lindgren J.A. Deficient lipoxin synthesis: a novel platelet dysfunction in myeloproliferative disorders with special reference to blastic crisis of chronic myelogenous leukemia. Blood. 78:1991;2989.
96. Stenke L., Nasman-Glaser B., Edenius C., Samuelsson J., Palmblad J., Lindgren J.A. Lipoxygenase products in myeloproliferative disorders: increased leukotriene C4 and decreased lipoxin formation in chronic myeloid leukemia. Adv. Prostaglandin Thromboxane Leukot. Res. 21B:1991;883.
97. Stenke L., Mansour M., Edenius C., Reizenstein P., Lindgren J.A. Formation and proliferative effects of lipoxins in human bone marrow. Biochem. Biophys. Res. Commun. 180:1991;255.
98. 4 analogues inhibit leukocyte recruitment to Porphyromonas gingivalis: a role for cyclooxygenase-2 and lipoxins in periodontal disease. Biochemistry. 39:2000;4761.
99. Maddox J.F., Colgan S.P., Clish C.B., Petasis N.A., Fokin V.V., Serhan C.N. Lipoxin B4 regulates human monocyte/neutrophil adherence and motility: design of stable lipoxin B4 analogs with increased biologic activity. FASEB J. 12:1998;487.
100. 4 receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J. Exp. Med. 191:2000;1197.
101. 4, and their analogs selectively downregulate PMN azurophilic degranulation. Am. J. Physiol. 276:1999;C988.
102. 4 stable analogs are demonstrable in human whole blood: modulation of leukocyte adhesion molecules and inhibition of neutrophil-endothelial interactions. Blood. 94:1999;4132.
103. 4 receptor that is regulated by IL-13 and IFN-γ and inhibits TNF-α-induced IL-8 release. J. Exp. Med. 187:1998;1285.
104. Dahlén B. Leukotrienes as Mediators of Asthma Induced by Aspirin and Allergen (Thesis). Stockholm: Department of Thoracic Medicine, Karolinska Institutet, 1993. p. 68.
105. Node K., Huo Y., Ruan X., Yang B., Spiecker M., Ley K.et al. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science. 285:1999;1276.
106. 4 inhibits IL-1 beta-induced IL-6, IL-8, and matrix metalloproteinase-3 production in human synovial fibroblasts and enhances synthesis of tissue inhibitors of metalloproteinases. J. Immunol. 164:2000;2660.
107. Godson C., Mitchell S., Harvey K., Petasis N.A., Hogg N., Brady H.R. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol. 164:2000;1663.
108. Shinmura K., Tang X.-L., Wang Y., Xuan Y.-T., Liu S.-Q., Takano H.et al. Cyclooxygenase-2 mediates the cardioprotective effects of the late phase of ischemic preconditioning in conscious rabbits. Proc. Natl. Acad. Sci. USA. 97:2000;10197.
109. 4 receptor. J. Exp. Med. 180:1994;253.
110. 4 receptors with aspirin-triggered 15-epi-LXA4 and regulation of vascular and inflammatory responses. Am. J. Pathol. 158:2001;3.
111. 4 receptor intracellular domains result in sustained signaling. Biochemistry. 39:2000;13551.
112. Godson C., Brady H.R. Lipoxins: novel anti-inflammatory therapeutics? Curr. Opin. Invest. Drugs. 1:2000;380.
113. 4. J. Immunol. 166:2001;3650.
114. McMahon B., Mitchell S., Brady H.R., Godson C. Lipoxins: revelations on resolution. Trends. Pharmacol. Sci. 22:2001;391.
115. Serhan C.N. Lipoxins and aspirin-triggered 15-epi-lipoxins are endogenous components of antiinflammation: emergence of the counterregulatory side. Arch. Immunol. Ther. Exp. 49:2001;177.